MicroRNA-7 inhibits epithelial-to-mesenchymal transition and metastasis of breast cancer cells via targeting FAK expression

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Kong, Xiangjun ^a   Li, Gaopeng ^a   Yuan, Yan ^a   He, Yan ^a   Wu, Xiaoli ^a   Zhang, Weijie ^a   Wu, Zhengsheng ^b   Chen, Tingting ^b   Wu, Wenyong ^b   Lobie, Peter E ^c   Zhu, Tao ^a  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b ANHUI MEDICAL UNIVERSITY   (China)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

FIBRONECTIN; FOCAL ADHESION KINASE; MATRIGEL; MESSENGER RNA; MICRORNA; MICRORNA 7; UNCLASSIFIED DRUG; UVOMORULIN; VIMENTIN;

ANCHORAGE INDEPENDENT GROWTH; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; BREAST EPITHELIUM; CANCER CELL; CANCER CELL CULTURE; CANCER INHIBITION; CANCER INVASION; CELL MIGRATION; CONTROLLED STUDY; CORRELATION ANALYSIS; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; METASTASIS; MONOLAYER CULTURE; MOUSE; NONHUMAN; PRIMARY TUMOR; PROTEIN EXPRESSION; PROTEIN TARGETING; REGULATORY MECHANISM; TUMOR GROWTH; TUMOR XENOGRAFT;

3' UNTRANSLATED REGIONS; ANIMALS; BASE SEQUENCE; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; DOWN-REGULATION; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; FOCAL ADHESION PROTEIN-TYROSINE KINASES; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICE; MICE, NUDE; MICRORNAS; NEOPLASM METASTASIS; PHENOTYPE; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84864422842     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0041523     Document Type: Article

References (54)

1. Bartel DP, ((2004)) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:: 281--297.
2. Ambros V, ((2004)) The functions of animal microRNAs. Nature 431:: 350--355.
3. Bartel DP, ((2009)) MicroRNAs: target recognition and regulatory functions. Cell 136:: 215--233.
4. Friedman RC, Farh KK, Burge CB, Bartel DP, ((2009)) Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19:: 92--105.
5. Ma L, Teruya-Feldstein J, Weinberg RA, ((2007)) Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 449:: 682--688.
6. Martello G, Rosato A, Ferrari F, Manfrin A, Cordenonsi M, et al. ((2010)) A MicroRNA targeting dicer for metastasis control. Cell 141:: 1195--1207.
7. Yao J, Liang L, Huang S, Ding J, Tan N, et al. ((2010)) MicroRNA-30d promotes tumor invasion and metastasis by targeting Galphai2 in hepatocellular carcinoma. Hepatology 51:: 846--856.
8. Valastyan S, Reinhardt F, Benaich N, Calogrias D, Szász AM, et al. ((2009)) A pleiotropically acting microRNA, miR-31, inhibits breast cancer metastasis. Cell 137:: 1032--1046.
9. Xiong Y, Fang JH, Yun JP, Yang J, Zhang Y, et al. ((2010)) Effects of microRNA-29 on apoptosis, tumorigenicity, and prognosis of hepatocellular carcinoma. Hepatology 51:: 836--845.
10. Park SM, Gaur AB, Lengyel E, Peter ME, ((2008)) The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev 22:: 894--907.
11. Kefas B, Godlewski J, Comeau L, Li Y, Abounader R, ((2008)) microRNA-7 inhibits the epidermal growth factor receptor and the Akt pathway and is down-regulated in glioblastoma. Cancer Res 68:: 3566--3572.
12. Webster RJ, Giles KM, Price KJ, Zhang PM, Mattick JS, et al. ((2009)) Regulation of epidermal growth factor receptor signaling in human cancer cells by microRNA-7. J Biol Chem 284:: 5731--5741.
13. Reddy SD, Ohshiro K, Rayala SK, Kumar R, ((2008)) MicroRNA-7, a homeobox D10 target, inhibits p21-activated kinase 1 and regulates its functions. Cancer Res 68:: 8195--8200.
14. Jiang L, Liu X, Chen Z, Jin Y, Heidbreder CE, et al. ((2010)) MicroRNA-7 targets IGF1R (insulin-like growth factor 1 receptor) in tongue squamous cell carcinoma cells. Biochem J 432:: 199--205.
15. Foekens JA, Sieuwerts AM, Smid M, Look MP, de Weerd V, et al. ((2008)) Four miRNAs associated with aggressiveness of lymph node-negative, estrogen receptor-positive human breast cancer. Proc Natl Acad Sci U S A 105:: 13021--13026.
16. Krek A, Grün D, Poy MN, Wolf R, Rosenberg L, et al. ((2005)) Combinatorial microRNA target predictions. Nat Genet 37:: 495--500.
17. Lewis BP, Burge CB, Bartel DP, ((2005)) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120:: 15--20.
18. Enright AJ, John B, Gaul U, Tuschl T, Sander C, et al. ((2003)) MicroRNA targets in Drosophila. Genome Biol 5:: R1.
19. Luo M, Guan JL, ((2010)) Focal adhesion kinase: a prominent determinant in breast cancer initiation, progression and metastasis. Cancer Lett 289:: 127--139.
20. Rehmsmeier M, Steffen P, Hochsmann M, Giegerich R, ((2004)) Fast and effective prediction of microRNA/target duplexes. RNA 10:: 1507--1517.
21. Siesser PM, Hanks SK, ((2006)) The signaling and biological implications of FAK overexpression in cancer. Clin Cancer Res 12:: 3233--3237.
22. Chu JH, Yu S, Hayward SW, Chan FL, ((2009)) Development of a three-dimensional culture model of prostatic epithelial cells and its use for the study of epithelial-mesenchymal transition and inhibition of PI3K pathway in prostate cancer. Prostate 69:: 428--442.
23. Migliore C, Petrelli A, Ghiso E, Corso S, Capparuccia L, et al. ((2008)) MicroRNAs impair MET-mediated invasive growth. Cancer Res 68:: 10128--10136.
24. Clark EA, Brugge JS, ((1995)) Integrins and signal transduction pathways: the road taken. Science 268:: 233--239.
25. Schaller MD, Borgman CA, Cobb BS, Vines RR, Reynolds AB, et al. ((1992)) pp125FAK a structurally distinctive protein-tyrosine kinase associated with focal adhesions. Proc Natl Acad Sci U S A 89:: 5192--5196.
26. McLean GW, Carragher NO, Avizienyte E, Evans J, Brunton VG, et al. ((2005)) The role of focal-adhesion kinase in cancer- a new therapeutic opportunity. Nat Rev Cancer 5:: 505--515.
27. Schlaepfer DD, Hanks SK, Hunter T, van der Geer P, ((1994)) Integrin-mediated signal transduction linked to Ras pathway by GRB2 binding to focal adhesion kinase. Nature 372:: 786--791.
28. Owens LV, Xu L, Dent GA, Yang X, Sturge GC, et al. ((1996)) Focal adhesion kinase as a marker of invasive potential in differentiated human thyroid cancer. Ann Surg Oncol 3:: 100--105.
29. Tremblay L, Hauck W, Aprikian AG, Begin LR, Chapdelaine A, et al. ((1996)) Focal adhesion kinase (pp125FAK) expression, activation and association with paxillin and p50CSK in human metastatic prostate carcinoma. Int J Cancer 68:: 164--171.
30. McCormack SJ, Brazinski SE, Moore JL Jr, Werness BA, Goldstein DJ, ((1997)) Activation of the focal adhesion kinase signal transduction pathway in cervical carcinoma cell lines and human genital epithelial cells immortalized with human papillomavirus type 18. Oncogene 15:: 265--274.
31. Kornberg LJ, ((1998)) Focal adhesion kinase expression in oral cancers. Head Neck 20:: 634--639.
32. Kornberg LJ, ((1998)) Focal adhesion kinase and its potential involvement in tumor invasion and metastasis. Head Neck 20:: 745--752.
33. Judson PL, He X, Cance WG, Van Le L, ((1999)) Overexpression of focal adhesion kinase, a protein tyrosine kinase, in ovarian carcinoma. Cancer 86:: 1551--1556.
34. Cance WG, Harris JE, Iacocca MV, Roche E, Yang X, et al. ((2000)) Immunohistochemical analyses of focal adhesion kinase expression in benign and malignant human breast and colon tissues: correlation with preinvasive and invasive phenotypes. Clin Cancer Res 6:: 2417--2423.
35. Lark AL, Livasy CA, Calvo B, Caskey L, Moore DT, et al. ((2003)) Overexpression of focal adhesion kinase in primary colorectal carcinomas and colorectal liver metastases: immunohistochemistry and real-time PCR analyses. Clin Cancer Res 9:: 215--222.
36. Gabriel B, Mildenberger S, Weisser CW, Metzger E, Gitsch G, et al. ((2004)) Focal adhesion kinase interacts with the transcriptional coactivator FHL2 and both are overexpressed in epithelial ovarian cancer. Anticancer Res 24:: 921--927.
37. Lark AL, Livasy CA, Dressler L, Moore DT, Millikan RC, et al. ((2005)) High focal adhesion kinase expression in invasive breast carcinomas is associated with an aggressive phenotype. Mod Pathol 18:: 1289--1294.
38. Agochiya M, Brunton VG, Owens DW, Parkinson EK, Paraskeva C, et al. ((1999)) Increased dosage and amplification of the focal adhesion kinase gene in human cancer cells. Oncogene 18:: 5646--5653.
39. Golubovskaya V, Kaur A, Cance W, ((2004)) Cloning and characterization of the promoter region of human focal adhesion kinase gene: nuclear factor kappa B and p53 binding sites. Biochim Biophys Acta 1678:: 111--125.
40. Felding-Habermann B, O'Toole TE, Smith JW, Fransvea E, Ruggeri ZM, et al. ((2001)) Integrin activation controls metastasis in human breast cancer. Proc Natl Acad Sci U S A 98:: 1853--1858.
41. Ruoslahti E, ((1999)) Fibronectin and its integrin receptors in cancer. Adv Cancer Res 76:: 1--20.
42. Valastyan S, Chang A, Benaich N, Reinhardt F, Weinberg RA, ((2010)) Concurrent suppression of integrin alpha5, radixin, and RhoA phenocopies the effects of miR-31 on metastasis. Cancer Res 70:: 5147--5154.
43. Müller DW, Bosserhoff AK, ((2008)) Integrin beta 3 expression is regulated by let-7a miRNA in malignant melanoma. Oncogene 27:: 6698--6706.
44. Mitra SK, Schlaepfer DD, ((2006)) Integrin-regulated FAK-Src signaling in normal and cancer cells. Curr Opin Cell Biol 18:: 516--523.
45. Ding J, Huang S, Wu S, Zhao Y, Liang L, et al. ((2010)) Gain of miR-151 on chromosome 8q24.3 facilitates tumour cell migration and spreading through downregulating RhoGDIA. Nat Cell Biol 12:: 390--399.
46. Wang HR, Zhang Y, Ozdamar B, Ogunjimi AA, Alexandrova E, et al. ((2003)) Regulation of cell polarity and protrusion formation by targeting RhoA for degradation. Science 302:: 1775--1779.
47. Zavadil J, Narasimhan M, Blumenberg M, Schneider RJ, ((2007)) Transforming growth factor-beta and microRNA:mRNA regulatory networks in epithelial plasticity. Cells Tissues Organs 185:: 157--161.
48. Zavadil J, Böttinger EP, ((2005)) TGF-beta and epithelial-to-mesenchymal transitions. Oncogene 24:: 5764--5774.
49. Cicchini C, Laudadio I, Citarella F, Corazzari M, Steindler C, et al. ((2008)) TGFbeta-induced EMT requires focal adhesion kinase (FAK) signaling. Exp Cell Res 314:: 143--152.
50. Yang Z, Rayala S, Nguyen D, Vadlamudi RK, Chen S, et al. ((2005)) PAK1 phosphorylation of snail, a master regulator of epithelial-to-mesenchyme transition, modulates snail's subcellular localization and functions. Cancer Res 65:: 3179--3184.
51. Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, et al. ((2008)) The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 10:: 593--601.
52. Wu DG, Wang YY, Fan LG, Luo H, Han B, et al. ((2011)) MicroRNA-7 regulates glioblastoma cell invasion via targeting focal adhesion kinase expression. Chin Med J (Engl) 124:: 2616--2621.
53. Park SI, Zhang J, Phillips KA, Araujo JC, Najjar AM, et al. ((2008)) Targeting SRC family kinases inhibits growth and lymph node metastases of prostate cancer in an orthotopic nude mouse model. Cancer Res. 68:: 3323--3333.
54. Heffron DS, Mandell JW, ((2005)) Opposing roles of ERK and p38 MAP kinases in FGF2-induced astroglial process extension. Mol Cell Neurosci 28:: 779--790.